Cumulative early life adversity predicts longevity in wild baboons

Abstract

In humans and other animals, harsh circumstances in early life predict morbidity and mortality in adulthood. Multiple adverse conditions are thought to be especially toxic, but this hypothesis has rarely been tested in a prospective, longitudinal framework, especially in long-lived mammals. Here we use prospective data on 196 wild female baboons to show that cumulative early adversity predicts natural adult lifespan. Females who experience ≥3 sources of early adversity die a median of 10 years earlier than females who experience ≤1 adverse circumstances (median lifespan is 18.5 years). Females who experience the most adversity are also socially isolated in adulthood, suggesting that social processes partially explain the link between early adversity and adult survival. Our results provide powerful evidence for the developmental origins of health and disease and indicate that close ties between early adversity and survival arise even in the absence of health habit and health care-related explanations.

Figure 1. Effect of cumulative early adversity on lifespan in female baboons.

(a) Survival curves using the full six factor cumulative adversity index (Wald test P=7.75 × 10⁻⁷, N=196); (b) Survival curves using a reduced four factor adversity index, without the effects of early maternal loss and competing younger sibling (Wald test P=0.004, N=196). Colours indicate the number of adverse conditions occurring in early life.

Figure 2. Relationship between lifespan and reproductive success.

Female baboons in Amboseli produce a single surviving offspring once every 2.13 years on average (based on the slope of the regression line), and do not exhibit extended post-reproductive lifespans. Surviving offspring are defined here as offspring who lived to at least age 1 (note that inter-birth intervals thus differ from estimates based on all offspring produced, which we used to define competing younger siblings). Among females in our data set who reached adulthood, lifespan explains 89.5% of the variance in the total number of surviving offspring (Pearson's r=0.946, P<2.2 × 10⁻¹⁶, N=72); thus, survival is a strong predictor of lifetime reproductive success.

Figure 3. Effect of early adversity on social connectedness during adulthood in female baboons.

Adult females that experienced high levels of early adversity were more socially isolated from (a) other adult females (LMM: P=0.005, n=123), but not from (b) adult males (LMM: P=0.503, n=123). The index of social connectedness on the y axis reflects the strength of female social connectedness relative to all other females alive in the population in the same year. High values indicate relatively high social connectedness, and low values indicate relative social isolation. Colours indicate the number of adverse conditions occurring in early life. Heavy lines in the middle of each coloured box mark the median, the top and bottom edges mark the 25th and 75th percentiles, and whiskers are the largest or smallest values at 1.5 times the interquartile range.